The station was owned and operated by Finnish railways until early 1918, when the last train, carrying station personnel and equipment, as well as some of the last Finns escaping revolutionary Russia, left for Finland. Later, ownership of the station was exchanged for Russian property in Finland, including the Alexander Theatre in Helsinki.

The station is famously known for the arrival of Vladimir Lenin by train from Switzerland on 3 April 1917 (O.S.). The event is commemorated by the Soviet statue of Lenin dominating the square in front of the station. This event is also referred to in the title of Edmund Wilson's book To the Finland Station (1940), a well-known study of revolutionary thought.

After the turmoil of the July Days, when workers and soldiers in the capital clashed with government troops, Lenin had to flee to Finland for safety, to avoid arrest. Lenin secretly returned from Finland disguised as a railway worker and protected by Eino Rahja and Alexander Shotman on 9 August 1917. Both times Lenin crossed the Russian–Finnish border on the engine #293 driven by Finnish engineer Hugo Jalava (Гуго Эрикович Ялава). The steam locomotive was donated by Finland to the Soviet Union in 1957, and is now installed as a permanent exhibit at one of the platforms on the station.

During the Siege of Leningrad in 1941–43, the Finland Station was the only Leningrad rail terminus that remained in use. The railway would connect Leningrad with a station near the western shore of Lake Ladoga, at which supplies from the non-occupied parts of the Soviet Union would arrive from across the lake, by boat or over the lake ice, via the so-called Road of Life.

In the 1950s, the old station building was demolished and replaced with a new one, inaugurated in 1960. The turreted building is decorated with sculptures glorifying the October Revolution and incorporates a portico preserved from the original 1870 edifice.

"West End Girls", a 1984 song by The Pet Shop Boys, contains the lyric "From Lake Geneva to the Finland Station". The song's co-writer, Neil Tennant, has a well-known interest and background in history (subject of his undergraduate degree), particularly that of Russia. This line refers to the train route taken by Vladimir Lenin when he was smuggled by the Germans to Russia during the First World War, a pivotal event in the Russian Revolution.[2]Edmund Wilson's book To the Finland Station, which Tennant most likely had read, may have also influenced this song's line.